The biology and ecology of the Pacific sharpnose shark Rhizoprionodon longurio

Abstract Amidst global declines in elasmobranch populations resulting predominantly from overfishing, the need to gather data regarding shark ecology is greater than ever. Many species remain data deficient or at risk of going extinct before sufficient conservation measures can be applied. In this review, we summarise existing knowledge regarding the biology and ecology of the Pacific sharpnose shark Rhizoprionodon longurio (Jordan & Hilbert, 1882), a small‐bodied carcharhinid shark found in coastal waters of the Eastern Tropical Pacific Ocean that is of both commercial and ecological importance. We compare ecological parameters of this species with its closest extant relatives and identify major knowledge gaps and avenues for future research. In particular, additional studies investigating the behavioural and sensory ecology, as well as potential migratory patterns of the species are needed. Such studies will not only improve our understanding of R. longurio, but provide insight into the extent to which the numerous studies performed on a close relative—Rhizoprionodon terraenovae—provide an accurate representation of the biology and ecology of Rhizoprionodon and carcharhinids more generally.

less accessible taxa should be a priority of contemporary shark research alongside efforts to categorise the population-level health of as many species as possible, ensuring that prioritisation of research effort can be made based on relative vulnerability to extinction.
Rhizoprionodon is a genus of small-bodied carcharhiniform sharks consisting of seven extant species distributed globally in tropical and temperate coastal waters (Compagno, 1984).Despite their conserved external morphology (Pinhal et al., 2012), Rhizoprionodon species exhibit clear differences in ecology and biology (Corro-Espinosa et al., 2011;Springer, 1964).R. terraenovae is by far the most intensively studied of the extant Rhizoprionodon species; however, the extent to which the characteristics of R. terraenovae are representative of the genus as a whole has not been assessed.
The Pacific sharpnose shark R. longurio (Jordan & Hilbert, 1882) is a comparatively understudied species found in shallow coastal waters of the Eastern Tropical Pacific Ocean from southern California to Peru (Compagno, 1984).Until recently, R. longurio was considered data deficient (Pinhal et al., 2012) and only in recent years has literature focussing on the species increased substantially.R. longurio is significantly more vulnerable to extinction than R. terraenovae on the basis of current IUCN estimates (Carlson et al., 2021;Pollom et al., 2020) and the species is subject to greater fishing pressure than R. terraenovae over much of its range (Corro-Espinosa et al., 2011;Pérez-Jiménez et al., 2015).For these reasons, improving our understanding of R. longurio biology and ecology is vital so that we may provide biologically informed conservation measures and maintain ecological function.
In this article, we summarise existing knowledge regarding the distribution, spatial ecology, growth, reproduction, trophic ecology and behaviour of R. longurio and provide comparisons to other members of the Rhizoprionodon genus.It has been 18 years since the last such review (Márquez-Farias et al., 2005), and during this time several studies have addressed previously unknown aspects of R. longurio ecology.As well as synthesising current knowledge, we comment on major knowledge gaps that constrain our understanding of the species and how they might be overcome.

| TA XONOMY AND E VOLUTION
Rhizoprionodon longurio is a small-bodied Carcharhiniform shark belonging to the genus Rhizoprionodon (Compagno, 1984).This genus is thought to have diverged approximately 53 million years ago (Carrier et al., 2012).As a relatively recent radiation, the genus Rhizoprionodon could prove a valuable case study for investigating the forces driving speciation in sharks.Several abiotic and biotic factors can drive such radiations (Simões et al., 2016;Solórzano et al., 2020); however, it is particularly challenging to identify these in ancient radiations where much subsequent evolution has occurred and patterns of genetic diversity can mask signatures of historical demographic events (Dudgeon et al., 2020;Richards et al., 2019).As well as the relatively recent nature of the Rhizoprionodon radiation, the geographical distribution of its constituent taxa warrants mention.
Genera such as Hemiscyllium, the speciation and biogeography of which has been focus of recent studies (Dudgeon et al., 2020) exhibit relatively restricted geographical distribution, whereas Rhizoprionodon taxa are found worldwide in the coastal waters of the Pacific, Atlantic and Indian oceans (Pinhal et al., 2012).Regardless, as of yet no studies have considered biogeography or speciation of the genus Rhizoprionodon specifically.
Rhizoprionodon taxa exhibit the 'typical' carcharhiniform body form (Sternes & Shimada, 2020;Thomson & Simanek, 1977); however, they differ from other carcharhinid sharks through a combination of morphological characters including enlarged hyomandibular pores and well-developed labial furrows (Springer, 1964), as well as the characteristic elongated snout from which the common name 'sharpnose shark' arises (Pinhal et al., 2012).The seven extant Rhizoprionodon species exhibit relatively conservative external morphology (Pinhal et al., 2012), however have previously been subdivided into two groups on the basis of features relating to vertebral centra morphology (Springer, 1964).Interestingly this taxonomic relationship is also recovered by molecular phylogenies (Naylor et al., 2012), through which Rhizoprionodon lalandii (another highly understudied species) can be defined as the sister taxon of R. longurio.R. longurio can also be distinguished from other Rhizoprionodon species morphologically since it has a relatively high tooth count, particularly elongated rostrum, characteristic upper labial furrow length and an absence of gyandric heterodonty (sexual dimorphism in dentition) (Springer, 1964).No existing studies expand on the potential for sexual dimorphism in R. longurio despite the abundance of sex-based morphological differences in other sharks and their potentially significant ecological and behavioural implications (Ritter & Amin, 2019;Whitehead et al., 2022).A lack of dental sexual dimorphism may suggest that sexual conflict is relatively weak compared with other elasmobranchs, however the absence of dental sexual dimorphism alone is insufficient to confirm this (Gayford, 2023).The morphological characteristics of R. longurio are relatively well understood compared with other aspects of the species' ecology, and therefore there are no major knowledge gaps in this area that are specific to R. longurio.Future morphological studies should examine the potential for morphological differences across the species' range, the genetic/developmental architecture underlying morphology and finescale morphological differences between the sexes and through ontogeny.

| DIS TRIBUTION AND MOVEMENTS
Understanding shark distribution and movement patterns is critical to ensuring their protection (Hammerschlag et al., 2011;Schlaff et al., 2014), as well as their ecological functions and interactions with other taxa (Bird, 2017;Tickler, 2021).R. longurio is found in the coastal waters of the Eastern Tropical Pacific Ocean, between Southern California and Perú (Figure 1; Compagno, 1984).It is the sole Rhizoprionodon species to inhabit this region, and in fact the only Rhizoprionodon species to live in isolation from all other members of the genus throughout its range (Pinhal et al., 2012).R. longurio is a benthopelagic species found in inshore waters in association with sandy and/or muddy substrates (Compagno, 1984;Corro-Espinosa et al., 2011;Márquez-Farias et al., 2005).Their ecology is broadly similar to other Rhizoprionodon species (Carlson et al., 2008;Munroe et al., 2014), although unlike R. taylori, R. longurio is not known to use seagrass habitats.This may be due to trophic differences between these species or due to a higher prevalence of sea grass habitats in the Western Pacific than the Eastern Tropical Pacific (Munroe et al., 2014;Short et al., 2001).Until recently, the habitat usage of R. longurio was unknown, however recent studies suggest that juveniles may utilise nursery areas for foraging purposes and/ or protection from potential predators (Trejo Ramírez, 2017).These are typically shallow, sheltered coastal regions including bays, mangroves and lagoons in which predation pressure is thought to be lower than the surrounding habitats (Heupel et al., 2007;Kinney & Simpfendorfer, 2009).Many carcharhiniform sharks, including some other Rhizoprionodon species are known to utilise nursery areas (Castro, 1993;Yokota & Lessa, 2006), and thus it is not surprising that R. longurio should engage in such behaviour.Intriguingly however, R. terraenovae is not thought to use shallow-water nursery areas, and instead juveniles of this species frequently occupy deeper waters, in some cases for extensive periods of time (Carlson et al., 2008).
Differences in the composition of respective communities, including differences in absolute predation pressure could be responsible for  (Kessel et al., 2014;Pratt & Carrier, 2001) and in many cases result in superficially similar patterns of dispersal and distribution (Parsons & Hoffmayer, 2005).In the case of R. longurio, migratory behaviour appears to be on a north-south axis (Alatorre-Ramirez et al., 2013;Márquez-Farias et al., 2005), however based on existing data inshore rather than latitudinal migration cannot be ruled out and future work should strive towards a greater understanding of these movements.Moreover, it is uncertain whether this migratory behaviour is observed across all size classes, or whether it is ontogenetically stratified (Gayford et al., 2023).R. longurio is often caught in gillnets (Márquez-Farias et al., 2005) which due to their mesh size would likely not capture smaller juveniles, meaning that data regarding seasonal variations in R. longurio distribution to date are only applicable to larger animals.Acoustic telemetry studies have been conducted for some Rhizoprionodon taxa, providing valuable information about their habitat usage, residency and abundance (Carlson et al., 2008;Munroe et al., 2014;Reyier et al., 2023).Regrettably, data regarding the movements and spatial ecology of R. longurio are scarce.In addition to the uncertainties regarding migratory behaviour, nothing is known about diel and vertical movements of this species besides vague speculation based on trophic studies (Alatorre-Ramirez et al., 2013;Osuna-Peralta et al., 2014).Future studies utilising acoustic and satellite telemetry data will provide F I G U R E 1 Map displaying the distribution of Rhizoprionodon longurio along the Western coast of The Americas, from Southern California to Perú.
better understanding about the spatial ecology of Rhizoprionodon species, which given their ecological and commercial importance (Corro-Espinosa et al., 2011;Pérez-Jiménez et al., 2015) should be a priority.In particular, effort should be made to characterise habitat usage of R. longurio in the Southern parts of its range, which as of yet remains entirely unknown.

| G ROW TH AND REPRODUC TI ON
Accurate information regarding the growth parameters of elasmobranch taxa is crucial for ensuring proper management (Harry, 2018;Smart et al., 2016).Furthermore, an understanding of a species' reproductive biology assists in determining its vulnerability to population declines (Bejarano-Álvarez et al., 2011;Carrier et al., 2004).
Sharks are typically thought of as k strategists exhibiting slow growth rates and low fecundity (Cortés, 2000), and as such are often thought of as being particularly vulnerable to extirpation (Dulvy et al., 2021).
The supposed dichotomy between r and k strategists in reality represents a continuum of life history strategies (Southwood et al., 1974) and there is considerable variation in fecundity and growth rates within Elasmobranchii (Cortés, 2000).Rhizoprionodon is a good example of this variation, thought to grow and mature rapidly compared with other elasmobranchs (Corro-Espinosa et al., 2011;Lessa et al., 2009).Even within Rhizoprionodon there is marked variation in growth parameters, with R. terraenovae thought to have a low rate of intrinsic population growth (Cortés, 1998;Márquez-Farias & Castillo-Geniz, 1998) compared with R. taylori (Simpfendorfer, 1999).
Until recently, detailed information regarding the growth functions of sharpnose sharks was restricted to only three of the seven extant species (Corro-Espinosa et al., 2011), and initial studies in R. longurio focused exclusively on the size distribution of individuals and length-weight relationships (Márquez-Farias et al., 2005).R. longurio is now thought to reach a maximum length of approximately 170 cm (Alatorre-Ramirez et al., 2013).Recent work has presented evidence that the species exhibits allometric growth in several key morphological structures, likely to have evolved as a result of ontogenetic niche shifts in diet and habitat use (Gayford et al., 2023).The most recent estimates of mean length at maturity are 100.61and 92.9 cm for males and females, respectively-the highest values reported for any Rhizoprionodon species (Corro-Espinosa et al., 2011).Observations of males maturing at greater length than females in R. longurio are particularly intriguing given that this is a viviparous species (Márquez-Farias et al., 2005).Females typically mature at greater lengths than males in viviparous elasmobranchs, with male-biased sexual size dimorphism observed predominantly in oviparous taxa (Colonello et al., 2020;Cortés, 2000).Female-biased sexual size dimorphism is thought to be associated with evolutionary constraint between fecundity and female body size (Colonello et al., 2020).As R. longurio matures at a larger size than its congeners (Corro-Espinosa et al., 2011), sex-specific selection on body size may be relaxed relative to other Rhizoprionodon species.Further work is required to elucidate the details of this relationship, and as a viviparous species exhibiting male-biased sexual size dimorphism, R. longurio represents an important data point for such studies.
Anatomical evidence suggests that R. longurio utilises the placental viviparity mode of reproduction, as do its congeners (Márquez-Farias et al., 2005).There is thought to be a single reproductive cycle per year (Corro-Espinosa et al., 2011), with gestation of approximately 10-12 months (Márquez-Farias et al., 2005;Mejía Salazar, 2007) and birthing occurring between the months of April and July (Corro-Espinosa et al., 2011).Litter sizes are thought to range between 1 and 12 embryos, with an average 7.4 embryos per litter (Márquez-Farias et al., 2005;Mejía Salazar, 2007).This is much higher than fecundity estimates for other Rhizoprionodon species (Capapé et al., 2006;Carlson & Baremore, 2003), and likely the major factor contributing to the resilience of the species to overfishing (Corro-Espinosa et al., 2011;Furlong-Estrada et al., 2015).No relationship between litter size and maternal size is known (Mejía Salazar, 2007), lending further credence to the absence of strong selection on female size at maturity.There does however appear to be substantial variation in embryo size within single litters (Márquez-Farias et al., 2005) as observed in other shark species (Schmidt et al., 2010).The genetic mating system of R. longurio still remains unknown and to date no studies have investigated the potential for polyandry or genetic monogamy in any Rhizoprionodon species.While not the only hypothesis (Braccini et al., 2007), multiple paternity or sperm storage could explain variations in embryo size and development (Pratt, 1993) in this species.Toxicology studies have found that macronutrients, essential trace elements and nonessential trace elements are all transferred placentally from mother to embryos in R. longurio (Baró-Camarasa et al., 2023;Frías-Espericueta et al., 2014).Importantly, the maternal transfer of nutrients is not identical for all elements, with some appearing in greater concentration in maternal tissues, and others in embryonic tissues (Baró-Camarasa et al., 2023;Frías-Espericueta et al., 2014).This could result from offloading of maternal toxins (Baró-Camarasa et al., 2023;Lyons et al., 2013;Mull et al., 2013), differential biochemical requirements of embryos and adults (Green, 2008;Swain & Nayak, 2009) or simply as a result of differences in the chemical properties different elements.
Further studies are needed to establish the biochemical details of nutrient transfer in R. longurio and the effects these may have on embryonic development and post-partum ontogeny.
Such movements may be more frequent in adults, with juveniles rarely targeting pelagic species (Alatorre-Ramirez et al., 2013).
Other Rhizoprionodon species such as R. taylori have been found to feed predominantly on pelagic species (Salini et al., 1998;Simpfendorfer, 1998), although even in this species the proportions of pelagic and benthic prey appear to vary geographically (Munroe et al., 2015).
There is some evidence for ontogenetic shifts in diet in R. longurio (Alatorre-Ramirez et al., 2013;Trejo Ramírez, 2017), although this is not consistent between all studies (Osuna-Peralta et al., 2014) and to date no evidence has been found to support sex-based differences in trophic ecology (Alatorre-Ramirez et al., 2013).Given apparent seasonal and geographical variation in trophic ecology, long-term trophic studies will be required to determine the extent to which ontogenetic trophic niche shifts are present.Such shifts have been documented in other Rhizoprionodon species (Bethea et al., 2006;Bornatowski et al., 2012) and it would not be surprising if similar trends occurred in R. longurio.Importantly, existing studies of trophic ecology in R. longurio are restricted to a very small proportion of its total range, predominantly due to lack of research effort.Considering the notable geographic variation in Rhizoprionodon trophic ecology, additional studies focussing on populations in the Southern half of R. longurio's range would provide the baseline of knowledge required to truly understand the trophic ecology of this species.
No studies have been conducted on these topics, and R. longurio is not commonly observed at any SCUBA or ecotourism sites, limiting potential to conduct long-term behavioural studies.Only a handful of studies exist regarding the sensory capabilities of any Rhizoprionodon species (Casper & Mann, 2009;Laforest et al., 2020), and there is no literature addressing fine-scale behavioural ecology of any members of the genus.Such studies have been conducted both in wild and laboratory-based populations of several small-bodied coastal shark species (Gruber & Myrberg Jr, 1977;Jordan et al., 2011;Stroud et al., 2014), and are crucial as they provide invaluable baseline data regarding how sharks interact with both the biotic and abiotic components of their external environment.There are currently no laboratory-held populations of R. longurio; however, nonexperimental approaches focussing on tagging and accelerometer data (as per Watanabe et al., 2019) would be easy to carry out with this species.Behavioural and sensory ecology remain understudied in the majority of elasmobranch taxa (Hueter et al., 2004) and thus in addition to providing key ecological information regarding R. longurio itself, such studies would help improve our understanding of taxonomic variation in elasmobranch sensory capabilities and behaviour.

| CON CLUS IONS
Researchers face a race against time to understand the biology and ecology of declining elasmobranch populations before they disappear entirely.R. longurio is a commercially significant species (Furlong-Estrada et al., 2015;Márquez-Farias et al., 2005) which also fulfils important ecological functions as a tertiary consumer (Alatorre-Ramirez et al., 2013).Several studies have discussed aspects of the ecology of R. longurio (Alatorre-Ramirez et al., 2013;Baró-Camarasa et al., 2023;Corro-Espinosa et al., 2011;Frías-Espericueta et al., 2014;Mejía Salazar, 2007;Trejo Ramírez, 2017); however, major gaps remain, particularly in the case of behavioural and sensory ecology.Deciphering the nature of the species' migratory behaviour should also be a key focus of future studies.All of these knowledge gaps can be reduced using existing technologies and methodologies that have previously been applied to other shark species.In the case of spatial ecology, acoustic/satellite tagging studies covering both sexes and both adults and juveniles would be sufficient to unravel the extent to which migratory behaviour is observed.In the case of behavioural/sensory ecology a more experimental approach may be required but given the small body size and coastal nature of this species it may well be amenable to temporary captivity.Crucially, existing studies are drawn from only a handful of populations, cumulatively covering a small percentage of the species' total range, and thus additional studies are needed to determine the extent to which R. longurio ecology is population-specific.Each of the future directions outlined here will not only improve our understanding of R. longurio and Rhizoprionodon ecology but provide a valuable contribution to our understanding of taxonomic variation in key ecological characteristics of cartilaginous fishes.

AUTH O R CO
such a difference.It is also plausible that, at least during this early ontogenetic stage, R. longurio and R. terraenovae are occupying different ecological niches.The most commonly stated observation regarding R. longurio movement in available literature regards a supposed northward seasonal migration in populations inhabiting the Gulf of California (Alatorre-Ramirez et al., 2013; Corro-Espinosa et al., 2011; Márquez-Farias et al., 2005; Osuna-Peralta et al., 2014).Unfortunately, little information is known about this putative migration, and such suggestions are based purely on fishing records and the tagging of a few individuals(Gayford et al., 2023;Kato & Carvallo, 1967).Seasonal variation in Rhizoprionodon catches is known from multiple species (Márquez-Farias et al., 2005; Parsons & Hoffmayer, 2005); however, the nature and drivers of these putative migrations remain uncertain.Both climate (temperature/ oxygen) and reproduction-driven migrations are plausible (Parsons & Hoffmayer, 2005) as both are known to occur in other elasmobranch taxa NTR I B UTI O N S Joel H. Gayford: Conceptualization (lead); writing -original draft (lead); writing -review and editing (lead).Darren A. Whitehead: Conceptualization (supporting); writing -original draft (supporting); writing -review and editing (supporting).